The spectral slope as a marker of excitation/inhibition ratio and cognitive functioning in multiple sclerosis
Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasi...
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| Vydané v: | Human brain mapping Ročník 44; číslo 17; s. 5784 - 5794 |
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| Hlavní autori: | , , , , , , |
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| Jazyk: | English |
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San Antonio
John Wiley & Sons, Inc
01.12.2023
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| ISSN: | 1065-9471, 1097-0193, 1097-0193 |
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| Abstract | Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro‐ and/or magnetoencephalography rolls off, is a non‐invasive biomarker of the E/I ratio. A steeper roll‐off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting‐state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (
p
= .01). In the sub‐cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (
p
= .01) and healthy subjects (
p
= .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS. |
|---|---|
| AbstractList | Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro‐ and/or magnetoencephalography rolls off, is a non‐invasive biomarker of the E/I ratio. A steeper roll‐off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting‐state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (
p
= .01). In the sub‐cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (
p
= .01) and healthy subjects (
p
= .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS. Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro- and/or magnetoencephalography rolls off, is a non-invasive biomarker of the E/I ratio. A steeper roll-off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting-state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (p = .01). In the sub-cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (p = .01) and healthy subjects (p = .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS.Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro- and/or magnetoencephalography rolls off, is a non-invasive biomarker of the E/I ratio. A steeper roll-off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting-state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (p = .01). In the sub-cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (p = .01) and healthy subjects (p = .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS. Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro‐ and/or magnetoencephalography rolls off, is a non‐invasive biomarker of the E/I ratio. A steeper roll‐off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting‐state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (p = .01). In the sub‐cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (p = .01) and healthy subjects (p = .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS. The 1/f slope enables us to pick up the inhibitory effect of benzodiazepines in people with multiple sclerosis (pwMS). Cognitively impaired pwMS also demonstrate a steeper 1/f slope, suggesting a decreased E/I ratio, and a stronger inhibition/weaker excitation when compared with cognitively preserved pwMS and healthy subjects. Multiple sclerosis (MS) is a neurodegenerative disease characterized by neuronal and synaptic loss, resulting in an imbalance of excitatory and inhibitory synaptic transmission and potentially cognitive impairment. Current methods for measuring the excitation/inhibition (E/I) ratio are mostly invasive, but recent research combining neurocomputational modeling with measurements of local field potentials has indicated that the slope with which the power spectrum of neuronal activity captured by electro‐ and/or magnetoencephalography rolls off, is a non‐invasive biomarker of the E/I ratio. A steeper roll‐off is associated with a stronger inhibition. This novel method can be applied to assess the E/I ratio in people with multiple sclerosis (pwMS), detect the effect of medication such as benzodiazepines, and explore its utility as a biomarker for cognition. We recruited 44 healthy control subjects and 95 pwMS who underwent resting‐state magnetoencephalographic recordings. The 1/f spectral slope of the neural power spectra was calculated for each subject and for each brain region. As expected, the spectral slope was significantly steeper in pwMS treated with benzodiazepines (BZDs) compared to pwMS not receiving BZDs (p = .01). In the sub‐cohort of pwMS not treated with BZDs, we observed a steeper slope in cognitively impaired pwMS compared to cognitively preserved pwMS (p = .01) and healthy subjects (p = .02). Furthermore, we observed a significant correlation between 1/f spectral slope and verbal and spatial working memory functioning in the brain regions located in the prefrontal and parietal cortex. In this study, we highlighted the value of the spectral slope in MS by quantifying the effect of benzodiazepines and by putting it forward as a potential biomarker of cognitive deficits in pwMS. |
| Author | Costers, Lars Nagels, Guy D'hooghe, Marie B. Van Schependom, Jeroen Akbarian, Fahimeh D'haeseleer, Miguel Rossi, Chiara |
| AuthorAffiliation | 5 Department of Neurology UZ Brussel Brussels Belgium 4 National MS Center Melsbroek Melsbroek Belgium 3 icometrix Leuven Belgium 1 Department of Electronics and Informatics (ETRO) Vrije Universiteit Brussel Brussels Belgium 2 AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium 6 St Edmund Hall University of Oxford Oxford UK |
| AuthorAffiliation_xml | – name: 1 Department of Electronics and Informatics (ETRO) Vrije Universiteit Brussel Brussels Belgium – name: 3 icometrix Leuven Belgium – name: 2 AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium – name: 4 National MS Center Melsbroek Melsbroek Belgium – name: 5 Department of Neurology UZ Brussel Brussels Belgium – name: 6 St Edmund Hall University of Oxford Oxford UK |
| Author_xml | – sequence: 1 givenname: Fahimeh orcidid: 0000-0002-1623-6005 surname: Akbarian fullname: Akbarian, Fahimeh organization: Department of Electronics and Informatics (ETRO) Vrije Universiteit Brussel Brussels Belgium, AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium – sequence: 2 givenname: Chiara surname: Rossi fullname: Rossi, Chiara organization: Department of Electronics and Informatics (ETRO) Vrije Universiteit Brussel Brussels Belgium, AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium – sequence: 3 givenname: Lars surname: Costers fullname: Costers, Lars organization: AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium, icometrix Leuven Belgium – sequence: 4 givenname: Marie B. surname: D'hooghe fullname: D'hooghe, Marie B. organization: National MS Center Melsbroek Melsbroek Belgium – sequence: 5 givenname: Miguel surname: D'haeseleer fullname: D'haeseleer, Miguel organization: National MS Center Melsbroek Melsbroek Belgium, Department of Neurology UZ Brussel Brussels Belgium – sequence: 6 givenname: Guy surname: Nagels fullname: Nagels, Guy organization: AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium, Department of Neurology UZ Brussel Brussels Belgium, St Edmund Hall University of Oxford Oxford UK – sequence: 7 givenname: Jeroen surname: Van Schependom fullname: Van Schependom, Jeroen organization: Department of Electronics and Informatics (ETRO) Vrije Universiteit Brussel Brussels Belgium, AIMS Lab Center for Neurosciences, Vrije Universiteit Brussel Brussels Belgium |
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| SubjectTerms | Autoimmune diseases Benzodiazepines Biomarkers Brain Cognition Cognitive ability Cognitive load Cortex (parietal) Disease Excitation Eye movements Inhibition (psychology) Language Magnetoencephalography Measurement methods Measurement techniques Multiple sclerosis Neurodegenerative diseases Parkinson's disease Power spectra Prefrontal cortex Scanners Schizophrenia Short term memory Sleep Spatial memory Synaptic transmission |
| Title | The spectral slope as a marker of excitation/inhibition ratio and cognitive functioning in multiple sclerosis |
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